W&M ScholarWorks VIMS Books and Book Chapters Virginia Institute of Marine Science 2005 Reproductive biology Christina L. Conrath Virginia Institute of Marine Science Follow this and additional works at: https://scholarworks.wm.edu/vimsbooks Part of the Aquaculture and Fisheries Commons Recommended Citation Conrath, Christina L., "Reproductive biology" (2005). VIMS Books and Book Chapters. 26. https://scholarworks.wm.edu/vimsbooks/26 This Book Chapter is brought to you for free and open access by the Virginia Institute of Marine Science at W&M ScholarWorks. It has been accepted for inclusion in VIMS Books and Book Chapters by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. FAO FISHER IES TECHNICAL PAPER 474 Management techniques for elasmobranch fisheries - VIMS SH 1 .F2 no.474 Asia-Pacific Economic Cooperation ~(nL; ,re..,~..., <SH j__ rJ, FAO VU) \\-y~ FISHERIES Management techniques ' TECHN ICAL PAPER for elasmobranch fisheries 474 Edited by John A. Musick Virginia Institute of Marine Science Gloucester Point, Virginia United States of America and Ramon Bonfil Wildlife Conservation Society New York United States of America FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS Rome, 2005 J/13 7. Reproductive biology Christina L. Conrath Virginia Institute of Marine Science PO Box 1346 Gloucester Point, VA 23062, USA <[email protected]> 7 .1 INTRODUCTION: MODES OF REPRODUCTION 7 .1.1 Introduction Several reproductive specializations are found within the elasmobranchs. All elasmobranchs fertilize internally and produce a relatively small number of large eggs. Elasmobranch fecundity generally ranges from one to two offspring produced a year up to a maximum of 300 in the whale shark (Compagno, 1990; Joung et al., 1996). Elasmobranch reproductive strategies include oviparity, aplacental viviparity and placental viviparity (Wourms, 1977). Oviparous species enclose eggs in an egg case and deposit them into the environment, where embryos develop external to the body of the mother. .Embryos remain in the egg case to develop for a period ranging from less than two months to over one year (Compagno, 1990). Viviparous species retain eggs within the uteri where the embryos develop. The yolk sac of placental viviparous species interdigitates with the uterine wall to form a placenta in which nutrients from the mother are transferred to the embryo. In most species the egg envelope is retained and incorporated into the uteroplacental complex (Hamlett, Wourms and Hudson, 1985). Gestation for viviparous species ranges from less than six months to greater than two years (Compagno, 1990). Viviparous species may have either lecithotrophic or matrotrophic development. Lecithotrophic development occurs when embryos derive their nutrition solely from yolk reserves and occurs in many aplacental viviparous species. Matrotrophic development occurs when embryos supplement the yolk reserves by obtaining maternally derived nutrients during gestation and also occurs in many aplacental species and all placental viviparous species (Wourms and Lombardi, 1992). The advantage of matrotrophy may be the increase in juvenile size at birth and therefore increased survivorship of young. Another important consideration in the evolution of elasmobranch reproductive strategies is the presence or absence of uterine compartments. Uterine compartments are formed in all species with placental development and some species with aplacental development and are believed to be an important step in the evolution of placental viviparity (Otake, 1990). 7.1.2 Oviparity Oviparity occurs in all batoids of the family Rajidae and six families and over 100 species of sharks in the orders Heterodontiformes, Orectolobiformes and Carcharhiniformes (Compagno, 1990; Compagno, 2001). In oviparous species, eggs are enclosed within an egg case and deposited in the sea. Two types of oviparity occur, extended oviparity and retained oviparity. Almost all oviparous species have extended oviparity in which large egg cases are fertilized , enclosed in an egg case, deposited and hatch after a period of up to 15 months. In this reproductive mode almost all of the embryonic development occurs within the egg case outside of the mother's body. Retained oviparity occurs 104 Manage~ent techniques for elasmobranch fisheries much more rarely and refers to species in which cased eggs are retained in the oviduct and development proceeds for a longer period before the eggs are released into the sea. One form of retained oviparity occurs in some scyliorhinid catsharks when multiple egg cases are retained within the oviduct before being released (Compagno, 1990; Compagno, 1988). The egg case generally has tendrils and sticky filaments that aide in attaching the egg to some sort of structure or substrate where the eggs incubate. The egg case also hardens after being deposited to protect the embryos from predation. All oviparous chondrichthyan eggs are laid in pairs (Mellinger, 1983 ). Oviparous embryos tend to be relatively smaller than viviparous embryos as growth of the embryo is constrained by the amount of yolk initially present in the yolk sac (Hamlett, 1997). Compagno (1990) suggests egg-laying clasmobranchs may select appropriate substrates for egg deposition as occurs in the bullhead shark in which the female picks up the egg after it is laid and wedges it into rocks or marine vegetation. Development time within the egg case is likely dependent on external temperature. Differences in the length of the incubation period of eggs laid by female thornback rays (Raja clavata), held at different temperatures have been noted in at least two aquarium experiments (Clark 1922, Ellis and Shackley 1995). 7.1.3 Aplacental viviparity Embryos from species with aplacental viviparous development are retained within the mother for the duration of development, but no placental connection is formed between the mother and the embryo. A wide range of developmental forms occur within this reproductive mode and Wourms (1977) separated them into three groups: those dependent entirely on yolk reserves, those which feed on other eggs or embryos and those which possess placental analogues. Animals within the first group are considered lecithotrophic as the embryo receives no extra nutrition from the mother and animals in the last two groups are considered matrotrophic as the embryo's nutrition is supplemented with either ovulated eggs or uterine milk (histotrophe). Aplacental yolk sacs Embryos from species within this group are entirely dependent on yolk reserves to complete development. This type of development is the most common reproductive strategy employed by sharks. It occurs in the orders Hexanchiformes, Squaliformes, Pristiophoriformes, Squatiniformes, Rhinobatiformes, Pristiformes, Torpediniformes and some species in the orders Orectolobiformes and Carcharhiniformes (Compagno, 1990). This form of development offers protection from predators for a longer period of time than oviparous development (Hamlett, 1997). Oophagy and adelphophagy Oophagy occurs when embryos within the uterus hatch out of the egg capsule after a few months and then consume additional eggs which continue to be ovulated while the embryo develops. Oophagy is thought to occur in all sharks in the order Lamniformes (Gilmore, 1993; Compagno, 1990). Specific examples described within the literature include the bigeye thresher shark (Alopias superciliosus), the pelagic thresher shark (A. pelagictts), the shortfin mako shark (lsttrus oxyrinchtts) and the porbeagle shark (Lamna nasus) (Moreno and Moron, 1992; Liu et al., 1999; Francis and Stevens, 1999; Mollet et al., 2000). In the sand tiger shark (Carcharias taurus), the first embryo to develop in each uterus consumes all the other embryos within that uterus (adelphophagy or intrauterine cannabilism) as well as additional ovulated eggs (Gilmore, Dodrill and Linley, 1983). This type of development may facilitate the development of large embryos and may prepare the embryo for a predatory life style (Wourms, 1977). Yano (1992) found that embryos of the false catshark (Pseudotriakis 7. Reproductive biology 105 microdon) also ingest yolk material from other ova but they transfer ingested yolk to an external yolk sac rather than forming the extended stomach of lamniform oophagous embryos. Female slender smooth-hounds (Collum attenuatus) form egg capsules which contain 30- 80 ova and only one ovum within each egg capsule develops. All other ova are ingested and packed to an external yolk sac (Yano, 1993). While ova arc ingested by the slender smooth-hound embryo during development, this form of reproduction may, or may not, be considered oophagy as after the initial consumption of ova within the egg sac, the embryo then develops without any additional ova or maternal investment. Placental analogues: histotrophe and trophonemata This type of development occurs in all rays of the order M yliobatiformes. Trophonemata are long villous extensions of the uterine epithelium that secrete histotrophc or "uterine milk" which can be ingested or absorbed by the embryo. The quantity and composition of the histotrophe varies widely between species. Trophonemata envelope the embryo and may occasionally enter the embryo through the spiracles. As yolk reserves are depleted, trophonemata increase in size and release uterine secretions rich in proteins and lipids (histotroph) (Wourms, 1981). White, Platell and Potter (2001) found that trophoncmata of the stingarec (Urolophus